Jasmonate-mediated wound signalling promotes plant regeneration

Abstract

Wounding is the first event triggering regeneration1,2,3,4. However, the molecular basis of wound signalling pathways in plant regeneration is largely unclear. We previously established a method to study de novo root regeneration (DNRR) in Arabidopsis thaliana5,6, which provides a platform for analysing wounding. During DNRR, auxin is biosynthesized after leaf detachment and promotes cell fate transition to form the root primordium5,6,7. Here, we show that jasmonates (JAs) serve as a wound signal during DNRR. Within 2 h of leaf detachment, JA is produced in leaf explants and activates ETHYLENE RESPONSE FACTOR109 (ERF109). ERF109 upregulates ANTHRANILATE SYNTHASE α1 (ASA1)—a tryptophan biosynthesis gene in the auxin production pathway8,9,10—dependent on the pre-deposition of SET DOMAIN GROUP8 (SDG8)-mediated histone H3 lysine 36 trimethylation (H3K36me3)11 on the ASA1 locus. After 2 h, ERF109 activity is inhibited by direct interaction with JASMONATE-ZIM-DOMAIN (JAZ) proteins to prevent hypersensitivity to wounding. Our results suggest that a dynamic JA wave cooperates with histone methylation to upregulate a pulse of auxin production and promote DNRR in response to wounding.

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Fig. 1: JA serves as a wound signal to promote DNRR.
Fig. 2: JA-ERF109-ASA1 wound signalling pathway in DNRR.
Fig. 3: SDG8-mediated H3K36me3 is involved in wound response.
Fig. 4: Prevention of hypersensitivity to JA-mediated wound signalling.

Data availability

The data that support the findings of this study are available from the corresponding author upon request.

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Acknowledgements

We thank the ABRC, Z. Zhu, G. A. Howe and D. Xie for providing the Arabidopsis seeds, Z. Zhu and W. Zhou for helpful discussion, Y. Liu from the Core Facility Centre of SIPPE for technical assistance on JA detection, and J. Pan and D. Cai for help on auxin concentration analysis. This work was supported by grants from the National Natural Science Foundation of China (31630007, 31770399 and 21375066), Strategic Priority Research Program of CAS (grant number XDB27030103), Key Research Program of CAS (QYZDB-SSW-SMC010), Youth Innovation Promotion Association of CAS (2014241 and 2014230) and National Key Laboratory of Plant Molecular Genetics.

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Contributions

G.Z., L.C. and L.X. designed the research. G.Z., F.Z. and Y.Z. performed the RNA-seq and ChIP-seq analyses. G.Z., Y.P., L.S. and N.B. analysed the auxin concentration. C.-X.C. and Z.Q. synthesized the COR-MO. L.Y. performed the Co-IP. G.Z., L.C. and T.Z performed the other experiments. G.Z., F.Z., L.Y. and L.X. analysed the data. L.X. wrote the article.

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Correspondence to Lin Xu.

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Journal peer review information: Nature Plants thanks Jian Xu and the other anonymous reviewers for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figures 1–7 and Supplementary Table 2.

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Supplementary Table 1

List of cluster-1 to -10 genes and JA- and auxin-related genes.

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Zhang, G., Zhao, F., Chen, L. et al. Jasmonate-mediated wound signalling promotes plant regeneration. Nat. Plants 5, 491–497 (2019). https://doi.org/10.1038/s41477-019-0408-x

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